At KPMG, he directed the office of general counsel, risk management, government affairs, security, and ethics and compliance programs.
He served as a law clerk to United States District Judge Thomas Rutherford Brett from 1980 to 1981.
Previously, Holmes was a partner at the law firm of Williams & Connolly in Washington, D.C., was staff director and general counsel to the Senate Select Committee on Intelligence from 1987 to 1989, Vice President of the Baltimore Orioles from 1989 to 1993, and administrative assistant to Governor David L. Boren of Oklahoma from 1975 to 1977.
Holmes was nominated by President Bill Clinton on September 22, 1994, to a seat vacated by Judge James O. Ellison.
In 2001, Chief Justice William Rehnquist appointed him to the Budget Committee for the Judicial Conference of the United States, where he served as vice chair from 2004 to 2005.